Depvartmient of Poultry Research, Ifye College (University of London), Ashford, Kent
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J. Anat. (1965), 99, 3, pp. 485-506 485 With 18 figures Prin#d in Great Brtiain The blood supply to the avian oviduct, with special reference to the shell gland BY R. D. HODGES Depvartmient of Poultry Research, IFye College (University of London), Ashford, Kent INTRO D U CT ION Until recently there was no detailed account of the blood supply to the avian shell gland. This situation was partially rectified by Freedman (1962) and Freedman & Sturkie (1963). Previous to this the only traceable accounts of the blood supply to the oviduct as a whole were those of Barkow (1829), Neugebauer (1845), Owen (1866), Streseman (1928), Mauger (1941) and Bradley & Grahame (1960), and to the shell gland in particular, those of Neugebauer (1845), Streseman (1928) and Hun- saker (1959). None of these accounts dealt with the subject in any detail. The shell gland withdraws the main component of the shell, calcium carbonate, from its blood supply in the form of calcium and carbonate ions at the same time that the shell is being laid down; there being no storage of calcium in the gland (Richardson, 1935). Consequently a detailed understanding of its vasculature is essential to any physiological investigations into the mechanism of shell secretion. The following account is an attempt to produce a detailed comparative study of the blood supply to the oviduct, and in particular the shell gland, of the three most common domesticated birds, the fowl, the turkey and the duck. MATERIALS AND METHODS The fowls (fifty-eight birds) used in this study were actively laying Light Sussex hens in the first or second laying season; the ducks (six birds) were mature breeding stock of the Aylesbury strain, and the turkeys (two birds) were actively laying Beltsville White hens. The majority of the birds, forty-nine fowls, the six ducks and the two turkeys, were injected with suspensions of red and blue neoprene latex (Neoprene Latex no. 572, Messrs Bostik Ltd., Leicester) in order to demonstrate the macroscopic and microscopic anatomy. The remaining nine fowls were injected with undiluted indian ink (Reeves waterproof indian ink) to demonstrate only the microscopic anatomy. The latex injection technique was as follows. The bird was killed with an intra- venous injection of pentabarbitone and the breast bone and liver removed. A poly- vinyl cannula was tied into the aorta below the heart and the blood was flushed out of the abdominal region with physiological saline warmed to 40° C., using a pressure of 2 ft. of water augmented by a manual pumping action on the supply tube. The latex was injected by means of an adaptation of the apparatus described by Tompsett (1956). A rubber hand bellows with a Winchester bottle reservoir and a mercury manometer were used as a pressure source in place of Tompsett's oxygen cylinder. The latex was injected at approximately normal blood pressures, i.e. 486 R. D. HODGES 1:30 mm. of mercury for the arteries and about 10 mm. of mercury for the veins. The arteries were injected with red latex through the aortic cannula, and the veinskere injected with blue latex by means of a cannula tied in the posterior vena cava. The latex coagulated in situ within an hour or so of injection. The latex casts of the blood vessels were obtained by corroding shell glands in concentrated hydrochloric acid for 72 hr. and then washing with water. Indian ink injections were made in the same way through the aorta, the ink passing through the capillary bed of the shell gland to fill the veins. All specimens were fixed and stored in 10 % formol saline. Portions of the ink-injected glands were examined in sections stained with Ehrlich's haematoxylin and eosin or by clearing with benzene and benzyl benzoate (Orsini, 1962). In both turkeys and three of the ducks the shell glands contained eggs. In the fowls forty-five glands contained eggs whilst the remaining thirteen were in the resting phase. Of the glands which contained eggs no attempt was made to differentiate the stages of shell formation. Although forty-nine of the fowls were injected with latex, in the following account the numbers cited frequently do not add up to this total, due partly to incomplete injections in some earlier cases and partly to vascular abnormalities in certain cases. The folds of the oviduct overlapped each other considerably, and in order to examine the blood supply closely it was necessary to cut the mesenteries. The diagrams represent the oviducts in a partially unfolded position; consequently manv of the vessels are elongated. NO MEN C LATURE Most of the nomenclature adopted in this account is that suggested by Freedman (1962) and Freedman & Sturkie (1963). Where the present author differs from these authors on points of nomenclature, the subject is discussed. Table 1. Explanation of newly named blood vessels Vessel Origin Distribution or drainage Anterior oviducal artery and The ovarian vessels Infundibulum and anterior vein magnum Middle uterine artery Femoral artery Most of magnum Middle uterine veins (except Renal rehevens vein Infundibulum, magnum and hypogastric) isthmus Inferior oviducal artery and vein Numerous points of Ventral surface of oviduct, origin (see text) excluding shell gland and vagina Superior oviducal artery and Numerous points of Dorsal surface of infundibulum, vein origin magnum and isthmus Utero-vaginal artery and vein Posterior uterine artery Posterior areas of shell gland and and vein utero-vaginal junction Vaginal arteries and veins Left pelvic artery or vein MNIiddle and posterior regions of the vagina Some previously undesignated vessels, particularly oviduct vessels, have been named. These, together with their origin and termination, are listed in Table 1. In order that the nomenclature shall correspond as closely as possible with that Blood supply of the avian oviduct 487 of Freedman & Sturkie (1963) all shell gland vessels will be termed 'uterine vessels'. However, throughout this account the terms shell gland and uterus are synonymous. Frequent mention has been made of the lateral and medial surfaces of the shell gland. When describing vessels of a particular surface the full designation is often complicated, e.g. the lateral lateral uterine artery. In these circumstances the shell gland surface will be given first and with a capital letter, thus the Lateral lateral uterine artery. RESULTS The blood supply to the oviduct Figure 1 is a diagram of the main blood vessels of the left side of the fowl's abdomen and the branches of these vessels which supply the oviduct. / I V - > ~~~~~;tiduct Cloaca) Fig. 1. Semi-diagrammatic representation of a ventral view of the abdominal blood vessels of the fowl and the branches supplying the oviduct and ovary. The oviduct has been displaced to the right making the oviduct vessels longer than normal. The kidney is shown in outline only. A, Anterior oviducal artery; B, hypogastric artery; C, left internal iliac artery; D, middle oviducal artery; E, anterior oviducal veins; F, middle oviducal veins; G, hypogastric vein; H, left internal iliac vein; J, inferior oviducal artery and vein; K, inferior uterine artery and vein; L, branches of anterior oviducal artery supplying inferior oviducal artery; M, lateral anterior uterine artery and vein; N, superior oviducal artery and vein; 0, dorsal aorta; P, renolumbar artery; Q, femoral artery; R, sciatic artery; S, ovarian artery; T, ovarian veins; U, renal rehevens vein; V, renal portal vein; W, pudendal artery and vein; X, posterior uterine artery and vein; Y, vaginal artery and vein; Z, pelvic artery and vein; DM, dorsal mesentery; ViM, ventral mesentery. 488 R. D. HODGES The blood supply to the oviduct in the fowl, turkey and duck is shown dia- grammatically in Figs. 2-4 respectively. Variations from the normal pattern of vessels in the fowl are shown in Fig. 5. The blood supply was found to be very similar in all three species. EF w Infundibulum ± Magnum i Isthmus w Shell gland w Vagina Fig. 2. Blood supply to the fowl's oviduct; normal pattern of vessels. Key as in Fig. 1. In Figs. 2-5 the method of representation of the blood vessels is as follows. The cross- hatched vessels are unaccompanied arteries; the black vessels are veins unaccompanied by arteries; and the white vessels represent arteries and veins running in parallel. Thus when an artery and vein meet, if the vessels passing away from the junction are white, it indicates that both the original vessels have divided to send parallel branches along the white vessels (Fig. 2, B, F). If, however, the artery and vein continue in their original state after the junction (Fig. 5, D, F) then this indicates merely a crossing over of vessels. Fig. 3. Blood supply to the turkey's oviduct; normal pattern of vessels. Key as in Fig. 1. The fowl Branches of the ovarian, hypogastric, femoral and left internal iliac arteries supplied the oviduct as follows: (1) A branch of the ovarian artery left the ovary and, coursing posteriorly along the surface of the anterior lobe of the left kidney, passed into the dorsal mesentery Blood supply of the avian oviduct 489 where it divided up to supply the infundibulum and anterior magnum (Fig. 2, A). This artery was termed the anterior oviducal artery. (2) In two out of the ten cases a branch of the left femoral artery passed between the anterior and middle lobes of the kidney and divided up to supply the middle and posterior magnum (Fig. 5, D). Although atypical, this vessel has been de- scribed by 'Mauger (1941) and was designated the middle oviducal artery. D F Fig. 4. Blood supply to the duck's oviduct; normal pattern of vessels.